Defective proviruses rapidly accumulate during acute HIV-1 infection

Nature Medicine

Volumn 22, Issue 9, 2016, Pages 1043-1049

  Bruner, Katherine M ^a   Murray, Alexandra J ^a   Pollack, Ross A ^a   Soliman, Mary G ^a   Laskey, Sarah B ^a   Capoferri, Adam A ^a,b   Lai, Jun ^a   Strain, Matthew C ^c   Lada, Steven M ^d   Hoh, Rebecca ^e   Ho, Ya Chi ^a   Richman, Douglas D ^c,d,f   Deeks, Steven G ^e   Siliciano, Janet D ^a   Siliciano, Robert F ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CD4 ANTIGEN; CYTIDINE DEAMINASE; ENVELOPE PROTEIN; GAG PROTEIN; GENOMIC DNA; GUANINE; INTERFERON;

ADULT; ANTIVIRAL THERAPY; ARTICLE; BIOACCUMULATION; CD4+ T LYMPHOCYTE; CHEMICAL COMPOSITION; CLINICAL ARTICLE; DISEASE COURSE; DNA DETERMINATION; ENVELOPE GENE; GENOME ANALYSIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; POLYMERASE CHAIN REACTION; POPULATION; PRIORITY JOURNAL; PROVIRUS; VIRUS GENOME; VIRUS RECOMBINATION; ACUTE DISEASE; AGED; BAYES THEOREM; COHORT ANALYSIS; FEMALE; HIV INFECTIONS; MALE; METABOLISM; MIDDLE AGED; VIROLOGY; VIRUS LATENCY; VIRUS LOAD; VIRUS REPLICATION; YOUNG ADULT;

ACUTE DISEASE; ADULT; AGED; ANTI-HIV AGENTS; BAYES THEOREM; CD4-POSITIVE T-LYMPHOCYTES; COHORT STUDIES; DISEASE PROGRESSION; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; PROVIRUSES; VIRAL LOAD; VIRUS LATENCY; VIRUS REPLICATION; YOUNG ADULT;

EID: 84981217035     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4156     Document Type: Article

References (43)

1. Finzi, D. et al. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278, 1295-1300 (1997).
2. Chun, T.W. et al. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. USA 94, 13193-13197 (1997).
3. Wong, J.K. et al. Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278, 1291-1295 (1997).
4. Siliciano, J.D. et al. Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells. Nat. Med. 9, 727-728 (2003).
5. Ruelas, D.S. & Greene, W.C. An integrated overview of HIV-1 latency. Cell 155, 519-529 (2013).
6. Ho, Y.-C. et al. Replication-competent non-induced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell 155, 540-551 (2013).
7. Finzi, D. et al. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat. Med. 5, 512-517 (1999).
8. Crooks, A.M. et al. Precise quantitation of the latent HIV-1 reservoir: implications for eradication strategies. J. Infect. Dis. 212, 1361-1365 (2015).
9. Archin, N.M. & Margolis, D.M. Emerging strategies to deplete the HIV reservoir. Curr. Opin. Infect. Dis. 27, 29-35 (2014).
10. Deeks, S.G. HIV: shock and kill. Nature 487, 439-440 (2012).
11. Archin, N.M. et al. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487, 482-485 (2012).
12. Siliciano, J.D. & Siliciano, R.F. Enhanced culture assay for detection and quantitation of latently infected, resting CD4+ T cells carrying replication-competent virus in HIV-1-infected individuals. Methods Mol. Biol. 304, 3-15 (2005).
13. Laird, G.M. et al. Rapid quantification of the latent reservoir for HIV-1 using a viral outgrowth assay. PLoS Pathog. 9, e1003398 (2013).
14. Strain, M.C. et al. Highly precise measurement of HIV DNA by droplet digital PCR. PLoS One 8, e55943 (2013).
15. Rouzioux, C., Mélard, A. & Avéttand-Fénoël, V. in Human Retroviruses (eds. Vicenzi, E. & Poli, G.) 1087, 261-270 (Humana Press, 2013).
16. Henrich, T.J., Gallien, S., Li, J.Z., Pereyra, F. & Kuritzkes, D.R. Low-level detection and quantitation of cellular HIV-1 DNA and 2-LTR circles using droplet digital PCR. J. Virol. Methods 186, 68-72 (2012).
17. Eriksson, S. et al. Comparative analysis of measures of viral reservoirs in HIV-1 eradication studies. PLoS Pathog. 9, e1003174 (2013).
18. Günthard, H.F. et al. Antiretroviral treatment of adult HIV infection: 2014 recommendations of the International Antiviral Society-USA Panel. J. Am. Med. Assoc. 312, 410-425 (2014).
19. Archin, N.M. et al. Immediate antiviral therapy appears to restrict resting CD4+ cell HIV-1 infection without accelerating the decay of latent infection. Proc. Natl. Acad. Sci. USA 109, 9523-9528 (2012).
20. Jain, V. et al. Antiretroviral therapy initiated within 6 months of HIV infection is associated with lower T cell activation and smaller HIV reservoir size. J. Infect. Dis. 208, 1202-1211 (2013).
21. Deng, K. et al. Broad CTL response is required to clear latent HIV-1 due to dominance of escape mutations. Nature 517, 381-385 (2015).
22. Delviks-Frankenberry, K. et al. Mechanisms and factors that influence high-frequency retroviral recombination. Viruses 3, 1650-1680 (2011).
23. Jetzt, A.E. et al. High rate of recombination throughout the human immunodeficiency virus type 1 genome. J. Virol. 74, 1234-1240 (2000).
24. Yu, H., Jetzt, A.E., Ron, Y., Preston, B.D. & Dougherty, J.P. The nature of human immunodeficiency virus type 1 strand transfers. J. Biol. Chem. 273, 28384-28391 (1998).
25. Hwang, C.K., Svarovskaia, E.S. & Pathak, V.K. Dynamic copy choice: steady state between murine leukemia virus polymerase and polymerase-dependent RNase H activity determines frequency of in vivo template switching. Proc. Natl. Acad. Sci. USA 98, 12209-12214 (2001).
26. Yu, Q. et al. Single-strand specificity of APOBEC3G accounts for minus strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11, 435-442 (2004).
27. Kieffer, T.L. et al. G->A hypermutation in protease and reverse transcriptase regions of human immunodeficiency virus type 1 residing in resting CD4+ T cells in vivo. J. Virol. 79, 1975-1980 (2005).
28. Pierson, T.C. et al. Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J. Virol. 76, 8518-8531 (2002).
29. Pillai, S.K. et al. Role of retroviral restriction factors in the interferon-α-mediated suppression of HIV-1 in vivo. Proc. Natl. Acad. Sci. USA 109, 3035-3040 (2012).
30. Harper, M.S. et al. Interferon-α subtypes in an ex vivo model of acute HIV-1 infection: expression, potency and effector mechanisms. PLoS Pathog. 11, e1005254 (2015).
31. Stacey, A.R. et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J. Virol. 83, 3719-3733 (2009).
32. Kearney, M.F. et al. Origin of rebound plasma HIV includes cells with identical proviruses that are transcriptionally active before stopping of antiretroviral therapy. J. Virol. 90, 1369-1376 (2016).
33. Maldarelli, F. et al. HIV latency. Specific HIV integration sites are linked to clonal expansion and persistence of infected cells. Science 345, 179-183 (2014).
34. Wagner, T.A. et al. HIV latency. Proliferation of cells with HIV integrated into cancer genes contributes to persistent infection. Science 345, 570-573 (2014).
35. Schröder, A.R.W. et al. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521-529 (2002).
36. Cohn, L.B. et al. HIV-1 integration landscape during latent and active infection. Cell 160, 420-432 (2015).
37. Simonetti, F.R. et al. Clonally expanded CD4+ T cells can produce infectious HIV-1 in vivo. Proc. Natl. Acad. Sci. USA 113, 1883-1888 (2016).
38. Bosque, A., Famiglietti, M., Weyrich, A.S., Goulston, C. & Planelles, V. Homeostatic proliferation fails to efficiently reactivate HIV-1 latently infected central memory CD4+ T cells. PLoS Pathog. 7, e1002288 (2011).
39. Massanella, M., Gianella, S., Lada, S.M., Richman, D.D. & Strain, M. Quantification of total and 2-LTR (long terminal repeat) HIV DNA, HIV RNA and herpesvirus DNA in PBMCs. Bio Protoc. 5, e1492 (2015).
40. Lorenzo-Redondo, R. et al. Persistent HIV-1 replication maintains the tissue reservoir during therapy. Nature 530, 51-56 (2016).
41. Rose, P.P. & Korber, B.T. Detecting hypermutations in viral sequences with an emphasis on G-> A hypermutation. Bioinformatics 16, 400-401 (2000).
42. Kim, M. et al. A primary CD4+ T cell model of HIV-1 latency established after activation through the T cell receptor and subsequent return to quiescence. Nat. Protoc. 9, 2755-2770 (2014).
43. Rosenbloom, D.I.S. et al. Designing and interpreting limiting dilution assays: general principles and applications to the latent reservoir for human immunodeficiency virus-1. Open Forum Infect. Dis. 2, ofv123 (2015).